Inorganic Particles Alter Competition in Grazing Plankton: The Role of Selective Feeding Author(s): Kevin L.

Kirk Reviewed work(s): Source: Ecology, Vol. 72, No. 3 (Jun., 1991), pp. 915-923 Published by: Ecological Society of America Stable URL: http://www.jstor.org/stable/1940593 . Accessed: 11/03/2013 20:22
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Ecology, 72(3), 1991, pp. 915-923 ? 1991 by the Ecological Society of Amenica

INORGANIC PARTICLES ALTER COMPETITION IN GRAZING PLANKTON: THE ROLE OF SELECTIVE FEEDING'
KEVIN L. KIRK2 Department ofBiological Sciences, Dartmouth NewHampshire College, 03755 USA Hanover,

Abstract. Suspended sediments(clay and siltparticles)differentially inhibitcladoceran populations, but not rotiferpopulations, and can change the outcome of competition between rotifers and cladocerans in favor of rotifers (Kirk and Gilbert 1990). This paper provides a mechanisticexplanationforthe population and community effects of suspended clay. Feeding experimentswith radioactivelylabeled phytoplankton cells (Cryptomonas) showed that the presence of suspended clay (<2-,gm particlesize) significantly decreased the phytoplankton ingestionratesof fivecladoceran species (Ceriodaphnia dubia, Daphnia ambigua, D. galeata mendotae,D. magna, and D. pulex) by 13-83% but not those of three rotifer species (Keratellacochlearis, K. crassa,and Synchaetapectinata).When radioactively labeled phytoplankton cells and clay particles were offered simultaneously,cladocerans wereless selectiveforphytoplankton over claythanwererotifers. Thus, cladoceransingested more suspended clay particlesthan did rotifers, and this caused the reductionsin phytoplankton ingestionrates. Smaller cladocerans were less selective forphytoplankton over clay thanwerelarger cladocerans,and theirphytoplankton rateswerethusreduced ingestion more by clay. Rotifersfed more selectivelythan eitherlarge or small cladocerans, were able to avoid ingesting clay particles,and therefore were not inhibitedby suspended clay. Thus, differences in the feedingmodes and selectivitiesof rotifers and cladocerans form the mechanisticbasis forthe change in competitiveoutcome in favorof rotifers observed in the presence of suspended clay. This mechanism may formthe basis forchanges in the relativeabundance of rotifers and cladocerans in turbidlakes and reservoirs. Keywords: Ceriodaphnia; cladocerans; competition; Daphnia; Keratella; rotifers; selectivefeeding; suspended clay;Synchaeta; zooplankton.
INTRODUCTION

A central idea in the study of competition is that changes in the environmentcan cause changes in the outcome of competition (Hutchinson 1978). Classic examples of this are given by Gause et al. (1934) in which the accumulation of metabolic waste products altered the directionof competitionbetween two species ofprotozoans,and by Park (1 9 54) in whichchanges in temperature and relative humidityaltered the direction of competition between two species of flour beetles. This approach can lead to a powerfulunderstandingof the process of competition,particularly if the mechanistic basis for the change in competitive outcome is known. For example, detailed knowledge of the physiologicaland population responsesof freshwater phytoplanktonspecies to changes in nutrient concentrations allowed Tilman (1982) to predicthow ratioschangedtheoutcome ofcomchangesin nutrient petitionbetweenphytoplankton species. Rotifersand cladocerans are two of the dominant I Manuscript 24 May 1990;revised received 3 September 1990;accepted17 September 1990. 2 Present address:Department of Biological Sciencesand Lake Superior Ecosystem Research Center, Michigan Technological University, Houghton, Michigan 49931 USA.

freshwater zooplankton groups.They compete exploitativelyformany of the same phytoplankton food resources,and largecladocerans (> 1.2 mm body length) mechanicallyinterfere withsmall, undefended rotifers. Large cladocerans are competitivelysuperiorto rotifers,and oftencause the suppressionor extinctionof rotifers (Gilbert 1988). Any physicalor biological factorthatdifferentially suppressescladoceransmorethan rotifers may cause a change in competitiveoutcome, and thus may change zooplankton communitystructure.In laboratorycompetitionexperiments, the presence of inorganic suspended sediment (clay and silt) particlesreversedthe usual competitivedominance of cladocerans over rotifers. In the absence of suspended clay, the rotifer Keratella cochleariswas outcompeted by the cladocerans Daphnia ambigua and Ceriodaphnia dubia. However, when suspendedclay was present, therotifer dominated the cultures, and the cladocerans were reduced to near extinction. The effectof suspended clay at the community level was explained mechanistically at thepopulation level: suspendedclay decreased the survivorship, and population fecundity, growthrates of cladocerans, but not of rotifers (Kirk and Gilbert 1990). Field observationssupportthe hypothesisthat suspended sediments affectzooplankton community

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916

KEVIN L. KIRK

Ecology, Vol. 72, No. 3

structure bychanging therelativeabundance ofrotifers and cladocerans in favorof rotifers. Cladoceran abundance is oftenlow in lakes that are turbid with suspended sediments (Adalsteinsson 1979, Hart 1986, Koenings et al. 1990). The relative abundance of rotifers and cladocerans in two basins of Lake Myvatn, a turbidlake in Iceland, appears to be determinedby suspended sediment concentration.In the less turbid D. longispina)dominate basin, cladocerans (primarily and rotifers are suppressed.In the more turbidbasin, cladocerans are rare and rotifers are abundant (Adalsteinsson 1979). in the feedingmodes, food-size niches, Differences and food-size selectivitiesof rotifers and cladocerans may be responsible for the differential effect of suspended clay on thesetwo groups.Herbivorous cladocerans rangein body size from0.3 to 3 mm. Most use a feeding mode formerly describedas filter feeding, but more accuratelydescribed as suspension feeding(e.g., et al. 1988). Metachronalmovementsoftheir Gerritson thoracic feedingappendages pump water throughan enclosed bronchialchamber, and suspended particles are collected by the setules of these appendages. Food particlesare thentransferred up a ventralfood groove to the mouth (Cannon 1933). Many particlesmay be captured,handled, and ingestedsimultaneously.Cladocerans ingestparticlesranging in size from0.5 to 40 Am (Burns 1968, DeMott 1982, 1985, Porter et al. 1983, Bogdan and Gilbert 1984, 1987, Gophen and Geller 1984). In addition, many cladocerans are nonselective feeders,and ingestparticlesin proportionto theirabundance in the environment(Lampert 1974, DeMott 1982, 1985, Brendelberger 1985). Because of theirrelatively nonselectivefeeding mode, and because the food-size niches of cladocerans overlap the range of suspended sedimentparticlesizes commonlyfound in nature(0.5-2 gin),cladoceransingestsuspendedsediments (Arruda et al. 1983, Gliwicz 1986). Ingestion of suspended sedimentparticlesreduces the ingestion rateson nutritious phytoplankton cells, perhapsdue to mechanicalinterference withthecollectionor ingestion of phytoplankton cells (Arruda et al. 1983, McCabe and O'Brien 1983, Hart 1988). This reductionin phytoplanktoningestionrate may cause the reductionsin cladoceran abundance oftenobserved in turbidlakes. Herbivorous rotifers are much smallerthan cladocerans (0.08-0.3 mm) and have a verydifferent feeding mode. Many rotifer species are raptorial.As theyswim the waterpropelled by bands of cilia on their through anterior end, they randomly encounter and capture individual preyitems,ranging in size from4 to 18 Am (Bogdan and Gilbert 1984, 1987, Gilbertand Bogdan 1984, Rothhaupt 1990). Thus, the food-size niche of rotifers is much narrower than thatof cladocerans and does notincludeparticlesin thesize rangeofsuspended sediments. In addition, rotifers feed selectively,and preferentially ingestlarge algal cells, particularly flagellates,over smalleralgal cells or bacteria (Bogdan and

Gilbert 1984, 1987, Gilbert and Bogdan 1984, Rothhaupt 1990). There are no data concerning the effects of suspended sedimentson the phytoplankton ingestion rates of rotifers, or on theirability to collect or ingestsuspended sediment particles.However, I suspect thatrotifers, because of theirselectivefeeding behavior and food-sizeniches,are able to avoid ingesting suspended sedimentparticles,and thus avoid the detrimentaleffects of suspended sediments. The overall goal of this paper is to understandthe mechanisms responsible for the differential effect of suspended clay on rotifer and cladoceran populations, and thus to determinethe mechanisticbasis for the changesin competitiveoutcome in thepresenceof suspended clay. I compare the effect of suspended clay on thephytoplankton ingestion ratesof a varietyof rotifer and cladoceran species. I also examine the selectivity of rotifers and cladocerans when feda mixtureof phytoplanktoncells and clay particlesas a way to quantify their relative abilitiesto ingest phytoplankton cellswhile avoiding clay particles.I testtwo hypotheses: that first, the phytoplankton ingestionrates of cladocerans, but not of rotifers, are decreased in the presence of suspended clay, and second, that rotifersselect phytoplankton cells over clay particles to a greaterextent thatdo cladocerans.The effect ofcladoceran body size, both withinand between species, is also considered.

METHODS

Clonal cultures of five cladoceran species (Ceriodaphnia dubia, Daphnia ambigua, D. galeata mendotae, D. magna, and D. pulex) and threerotifer species (Keratella cochlearisf. tecta,K. crassa, and Synchaeta pectinate) were maintained in the laboratoryat 20'C in glass-fiber-filtered pond waterand fed Cryptomonas sp. (isolated by John Gilbert). In order to obtain cladocerans of nearlyequal size, individuals of the same age (within 1 d) were used in all experiments;this resulted in a range of cladoceran body lengthstypically < I0% of the mean withinany given experiment. Stock suspensionsofclay werepreparedas described in Kirk and Gilbert(1990). Briefly, clay collectedfrom a soil sample was repeatedlyboiled in sodium hypochloriteto eliminate organic matter,washed by cenand size fractionated trifugation, by settling.Mineratheclay was composed ofa mixed-layer logically, illite/ smectite(R. Reynolds,personal communication).The coarse size fraction used here had a mean particlesize of 1 ,im, and 95% of the particleswere <2 ,im. A clay suspension produced by adding 50 mg dry mass per litreof watercontained 3.98 x 108particles/mL (Kirk and Gilbert 1990) and had a turbidityof 68 NTU (nephelometric turbidityunits) (J. Minor, personal communication). Each feedingexperiment, fora given rotifer or cladoceran species or size class, consisted of two treat-

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In the ments,with5-6 replicatebeakersper treatment. first treatment, animals were simultaneouslyexposed to labeled phytoplankton and labeled clay. This treatover ment enabled the selectivityfor phytoplankton clay to be determined.In the second, or control,treatment,animals were exposed to labeled phytoplankton without thepresenceofsuspendedclay. Phytoplankton ingestion ratesin thecontroland suspended clay treatmentswerecompared to determineto what extentthe the phytoplankton presenceof suspended clay affected coningestionrate. In all experimentsphytoplankton centration was 5000 cells/mL,and clay concentration was zero or 50 mg/L. Suspended clay concentrations of 50 mg/Lare common in shallowlakes and reservoirs (see Kirk and Gilbert 1990). wereconductedwith Dual-label feeding experiments cells and 3Hmixturesof 32P-labeledphytoplankton labeled clay particles, usingtechniquessimilarto those used by Lampert (1974), DeMott (1982), and Bogdan and Gilbert (1984). The phytoplankton species used, (Gilbertand Bogdan 1984), and was grownin unialgal batch culturesin modifiedMarine Biological Laboratory(MBL) medium (Stemberger1981). To radioactively label the Cryptomonas cells, 6 mL algal suspenCryptomonas sp., is an ovate cell 7 x 14,gm in length

sion of 6-8 d old cultures was diluted with 6 mL tubes. Two phosphate-free MBL in plastic centrifuge to fourMBq of carrier-free 32P-orthophosphate (New EnglandNuclear) was added to each tube,and thetubes were incubated under continuous illumination.After werewashed twiceby cen18-36 h, thephytoplankton and resuspended in 0.2-gimfiltered pond trifugation, of the resulting labeled stock water.The concentration suspension was determinedby countingcells in a heand the final labeled suspension was mocytometer, made by dilutingthe stock in 0.2-,gm filteredpond water. The clay was labeled by adsorbing 3H-lysine (New England Nuclear) onto the surfacesof the clay of a 2500 mg/Lclay suspenparticles.Ten millilitres sion were incubated with 200 Bq 3H-lysineat room for2 h on a rotaryshaker. The clay was temperature and resuspended then washed twice by centrifugation in filtered pond water. Animals were acclimated for 2-5 h in nonlabeled suspensions having the same algae and clay concentrationsthattheywould experienceduringthe feeding wereconductedat 200 period. Acclimationand feeding in a walk-inincubator,underfluorescent lights.During the acclimation period, 1-6 cladoceran individuals of a givenspecies (fewerindividuals forlargerbody sizes) were contained in 20-mL suspensions in 40-mL disindividualswere posable plasticbeakers;50-100 rotifer contained in 10-mL suspensions.The clay was kept in thebeakersby hand about suspensionbygently swirling every 30 min. To initiate a feedingperiod, an equal volume (10 or 20 mL) of labeled suspension was rapidly poured into a beaker containingacclimated animals. After a 5-minfeedingperiod,the contentsof the

beaker were poured through a Nitex net filter (200-gm mesh forcladocerans, 48-,4mmesh forrotifers) glued to the bottom of a plexiglass tube. Fifty-100 mL of ice-cold, carbonated water were poured throughthe filter to simultaneously rinseand narcotizetheanimals. Tubes containingcladocerans were plunged into icecold, carbonated water, and cladocerans were transferred with a pipetteto glass scintillationvials within 1 min. Rotifers werewashed with 1% buffered formalin into a petri dish, and transferred with glass micropipettes to scintillationvials within 5 min. Individuals froma singlereplicatefeeding beaker were placed into a singlescintillation vial. Animals were solubilized by adding 1 mL Protosol (New England Nuclear) to each vial and agitating on a rotaryshakerat room temperature for 1 d. Ten millilitresAquasol II scintillation cocktail(New England Nuclear) and fourdrops glacial acetic acid were added to each vial. The acid neutralized the basic Protosol and reduced chemiluminesthe vials sit for 1 d cence (DeMott 1982). Afterletting to eliminate any residual chemiluminescence,the radioactivityin each vial was assayed using a Beckman LS5800 liquid scintillationcounter. Quenching and counting efficiency weredetermined foreach vial using externalstandardization. Since the labeled phytoplankton and clay were present in the same suspension duringthe feedingexperiments,it is possible thatthe clay adsorbed 32P-labeled dissolved organic matterreleased by the labeled phytoplankton cells. In order to minimize this possible of clay with32P,the labeled phytoplankcross-labeling ton and clay were combined for only 1 min before they were used in an experiment.A preliminaryexoccurred.Five perimentshowed thatno cross-labeling thousand cells per millilitreof 32P-labeled Cryptomonas cells were incubated in 0.2-gm filtered pond water for4 h. The phytoplankton cells were thencentrifuged which contained 32P-labeled out, and the supernatant, dissolved organicmatter, was used in a feedingexperiment with unlabeled clay. D. ambigua fed this clay suspension showed no accumulation of radioactivity above backgroundcounts (K. L. Kirk,personal observations).Anotherpotentialcross-labeling problemmay occur because Cryptomonascells may themselvesingest 3H-labeled clay particles. Other Cryptomonas species have been shown on ingest small particles cells (Porteret al. 1985). However,since phytoplankton were in contact with 3H-labeled clay for only a short time, cross-labelingshould be insignificant. in algal ingestionrates betweenthe first Differences and second treatments(with and without clay) were analyzed usingt tests(Sokal and Rohlf 1981). Selective or the ingestionof a preyitem out of proporfeeding, was indexed tion to its abundance in the environment, using a (Chesson 1983). Possible values foraXA (selecforalgae) rangefrom0 (no algae eaten) to 1 (only tivity algae eaten). An aA of 0.5 indicates nonselectivefeedwas ing,and thenull hypothesis ofnonselectivefeeding

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918

KEVIN L. KIRK Algal Ingestion Rate (103 cells/h)

Ecology, Vol. 72, No. 3

0
Cl adocerans Ceriodaphnio dubic (0.98 mm) Dophnia ambiguc (1.33 mm) D. goleato mendotae (1.99 mm) D. mogno (1.23 mm) (2.26 mm) D.pulex (1.16 mm) (1.73 mm)
(2.74

20

40

60

***

**
*

0 Control * With clay

**

mm)

=:4

NS

(106

cells/h)

0
Rotifers Kerotello cochlearis K. cross Synchoeto pectinato

20

40

60

NS
NS

FIG. 1. Effect of 50 mg/L suspended clay on the algal (Cryptomonas)ingestionrates of five species of cladocerans and difference between are given in parentheses.Means + SE. t testsof significant threespecies of rotifers. Cladoceran body lengths and control:NS = not significant clay treatment (P > .05); **P < .01; ***P < .001.

analyzed using t tests to compare the observed Ca to ofsuspendedclay,whereasthatofyoungadult D. magbetweenaA values were na (2.26 mm) decreased by 50%. 0.5 (Chesson 1983). Differences seshowed significant All cladocerans and rotifers means test tested using Tukey's multiple-comparison cells over clay particles:aA lectivity forphytoplankton (SAS 1985). >0.5 forall animals (all P < values were significantly weremore selectivethan .05; Fig. 3). However, rotifers RESULTS ranged from0.855 to cladocerans. The aA forrotifers The phytoplankton ingestionratesof all fivespecies 0.997, whereastheaA for 0.688 cladoceransrangedfrom ofcladoceranswerereducedby 13-83% in thepresence to 0.827. Fig. 3 shows the resultsof Tukey's multipleof 50 mg/Lcoarse suspended clay (Fig. 1). These re- comparisonmeans testsfordifferences betweenaA valductions were statistically significant (P < .05) forall ues, using an experimentwise errorrate of 0.05 (SAS cladocerans except large (2.74 mm body length) D. K. crassa 1985). The aA values oftwo species ofrotifers, pulex. In contrast,the phytoplankton ingestionrates and S. pectinate(0.997 and 0.986, respectively), were of three species of rotifers were not significantly re- significantly different fromthoseofall cladoceranstestduced (Fig. 1). K. cochlearis(0.855) was siged. The aA of the rotifer different from those of young D. magna Smaller cladocerans were more inhibited by sus- nificantly pended clay than were largercladocerans. The percent (0.709) and adult C. dubia (0.688). Smaller cladocerans were less selective than larger inhibitionof phytoplankton ingestionrate was negativelycorrelatedwith cladoceran body size (P < .05; cladocerans; aA is positivelycorrelatedwithbody size Fig. 2A). Withina cladoceran species, the smaller,ju- (P < .0 1; Fig. 2B). This trendholds both betweenand venile individuals were more inhibitedby suspended within species. For example, the smallest cladoceran clay than were larger adults. For example, the algal species tested,C. dubia (0.98 mm), had the lowest seingestion rate of juvenile D. pulex (1.16 mm body lectivity(aA =0.688). For D. pulex, as body size inlength)decreased by 68% in the presenceof suspended creased from 1.16 to 2.74 mm, selectivityincreased clay, whereas that of young adult D. pulex (1.73 mm) from0.759 to 0.827. For D. magna, as body size indecreased by 49%. The algal ingestionrate ofjuvenile creased from 1.23 to 2.26 mm, selectivityincreased D. magna (1.23 mm) decreased by 74% in thepresence from0.709 to 0.779.

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June 1991
DISCUSSION

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Inhibitionof algal feedingrate The resultsclearlysupportthe first hypothesis:suspended clay reduced the algal ingestion rates of all cladoceranspeciestested, butnone oftherotifer species tested(Fig. 1). No previousworkhas been done on the effect of suspended sedimentson the feedingrates of rotifers, but other investigators have shown that suspended sediments reduce the algal ingestionrates of cladocerans. Arruda et al. (1983) found that the algal ingestionrates of D. parvula and D. pulex were decreased in the presenceof suspended sedimentsat concentrations>50 mg/L. McCabe and O'Brien (1983) found that the algal ingestion rate of D. pulex was reduced at suspended sediment concentrations>10 NTU. Hart (1988) foundthatthe ingestionratesof D. gibba, D. barbata, and D. longispinadecreased as suspended sediment concentrationsincreased above 55 NTU. In contrastto these results,Koenings et al. (1990) presentdata that suggestthat the algal ingestionrate of D. galeata mendotaewas increased in the presence of suspended sediments.However, theydid not meabut estimated it by measure ingestionrate directly, suring therateofdeclinein chlorophyll a concentration in jars containingcladocerans. Chlorophylla concenabuntrationwas used as an index of phytoplankton dance. The rate of decline in chlorophylla over a 2-d period was two times greaterin jars containingsuspended glacial flourparticles (1-30 jim) than in jars without suspended sediments. They attributedthese resultsto higheralgal feedingrates by the cladocerans in thepresenceofsuspendedsediments.However,their experiments had no controls, without cladocerans. Therefore, an alternative explanation is thatthe direct effectsof suspended sediments on phytoplankton on cladoceran feedabundance, ratherthan the effects a ing,caused the greaterrate of decline of chlorophyll in jars containingsuspended sediments.For example, suspended sediments may have reduced light levels, in phytoplankton rate causingreductions photosynthesis (Grobbelaar 1985), or reductionsin the concentration of chlorophylla per cell. The differential of suspended clay on rotifers effect and cladoceransis also observed at clay concentrations >50 mg/L.The algal ingestionrate of the cladoceran D. ambigua was reduced by 87% by 200 mg/L susS. pectinate rateoftherotifer pended clay;theingestion was unaffected (K. L. Kirk,personal observations). Selectivefeeding The results from the treatmentin which animals weresimultaneously presented withalgae and clay suprotifers weremoreselective portthesecond hypothesis:

c)

Cd

8
-

a)

C A

A D

C
)

6040-

D
L)a
A

A Ca

A C

C 0
U

204

D;D

-o

La:
0.9
A A

a)

0.5

1.0

1.5

2.0

2.5

3.0 B

0.8
A A A

0.7

0.6 0.5

1.0

i.5

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2.5

3.0

Cladocercn Body Length (mm) 2. (A) Relationship between meancladoceran body inalgalingestion length and percent inthepresdecrease rate enceof 50 mg/L to controls without clayas compared clay. rank Spearman's correlation coefficient 1981), (SokalandRohlf
FIG.

r, = 0.85; P < .01. Species abbreviations: Cd Ceriodaphnia dubia; Da Daphnia ambigua; Dgm D. galeata mendotae;Dm D. magna; Dp D. pulex.

eran bodylength andmeanselectivity for algaeoverclay(A).

r = -0.72; P < .05. (B) Relationship between mean cladoc-

foralgae over clay than were cladocerans (Fig. 3). This in previous studies of the relative patternis reflected size-selectivities of rotifers and cladocerans when fed mixtures of small and largeparticles.Cladocerans, particularly daphnids,ingestsmall (< 2 gm) as well as large particles(DeMott 1982, 1985, Porteret al. 1983, Bogdan and Gilbert 1984, 1987, Gophen and Geller 1984), whilemost rotifers do not ingestparticles< 4 Am(Bogdan and Gilbert 1984, 1987, Gilbertand Bogdan 1984, Rothhaupt 1990). Nonselective feedingwas correlatedwithreductions in algal ingestionrate in the presence of clay. Those animals thatwere less selective foralgae over clay are more inhibitedby the presence of suspended clay (P < .01; Fig. 4). In particular,cladocerans are less selective than rotifers, and the algal ingestionrates of cladocerans,but not ofrotifers, are reducedin thepresence of suspended clay. Suspended clay reduces cladoceran feedingrates by interfering with the collection and ingestionof algal cells. Cladocerans ingestlarge amounts of suspended

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920

KEVIN L. KIRK
atA

Ecology, Vol. 72, No. 3

0.6 Cladocerans Ceriodophniodubic (0.98 mm) Dophniu ombiguc (1.33 mm) D. galeoto mendotoe (1.99 mm) D. mogna (1.23 mm) (2.26 mm) D. pulex (.16 mm) (1.73 mm) (2.74 mm) Rotifers Kerotella cochlecris K. cross Synchoeta pectinoto

0.7
A

0.8

0.9

1.0

A,B B A

B A, A,B A,B B

W C C

FIG. 3. Selectivityforalgae (aA) of fivespecies of cladocerans and threespecies of rotifers when simultaneouslyoffered algal cells (Crvptomonas)and suspended clay particles.An asA of 0.5 indicates nonselectivefeeding;an asA of 1.0 indicates ingestionof only algal cells. Means + SE. Bars labeled with the same letterare not significantly different (Tukey's multiple comparison means test,experimentwise errorrate = 0.05).

clay,as shownby theirrelatively low selectivity values. The presence of large amounts of suspended clay in the gut causes a reductionin the rate of thoracic appendage beating, decreasing the amount of water pumped through the bronchialchamber,and thus decreasingalgal ingestionrate.In addition,collectedclay particles clog the food groove in the region near the mouth and cause the rejection of boluses containing both algae and clay, also decreasingthe algal ingestion rate (Kirk 1988). Thus, collected and ingested suspended clay particlesreducecladoceran phytoplankton feeding ratesby mechanicallyinterfering withboth the collection and ingestionof phytoplankton cells. Althoughrotifers were more selective than cladocerans,bothgroupsselectedalgae over clay: all aA values were significantly >0.5 (Fig. 3). It is likely that this selective feedingon algal cells is passive, not active. Passive prey selection resultsfromdifferences in the ability of a predator to encounter,capture, or ingest different preyitems.In active preyselection,a predator encounters a preyitem,and is able to eat it,but avoids or rejects it (Gilbert 1980). Most rotifer species, because of their raptorial feeding mode and the morphologyof theirfeedingapparatus,simplycannot capturesmall items such as clay particlesor bacterialcells (Gilbertand Bogdan 1984). Thus, the observed selection of algal cells by rotifers may be passive. Active selectionby rotifers cannot be ruled out, however. Rejection of clay particlesafter collection,perhapson the basis of taste (DeMott 1986), is one possible mechanism foractive selection.Cladocerans collectlargepar-

tides (>2 gim)such as algal cells on theirthoracicappendages withgreater efficiency than smallerparticles, such as clay. Thus, algal cells are capturedat a greater rate. Cladocerans have no mechanism forsorting capturedparticles, or forselectively rejecting clay particles priorto ingestion, so theyare unlikely to exhibitactive preyselection. The success of a suspension-feeding zooplankterin the pelagic environmentdepends upon its ability to ingestnutritious particleswhileavoidingnonnutritious or toxic particles.In nature,phytoplankton and bac0

100

.
U)

80 60

A A

c:
_

AA

40
o 20

'

0.6

0.7

0.8

0.9

.0

FIG. 4. Relationship between mean selectivity (aA) and in algalingestion percent decrease ratein thepresence of 50 mg/L coarseclay,forcladocerans (A) and rotifers (-). r, = -0.78; P < .01.

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June 1991

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entlyto suspended clay. Both withinand betweenspecies, smaller cladocerans are less selective than larger cladocerans, and, as a result,are more inhibited by in the mesh sizes suspended clay (Fig. 2). Differences of the thoracicfeeding appendages, or the distance between the setules involved in particle capture, may account forthis trend. Geller and Muller (1981) and Brendelberger and Geller (1985) found that the thoracic appendage mesh size of many Daphnia species increaseswithincreasingbody size. Althoughthoracic appendage mesh size is not the only determinantof food-sizeselectivity et al. 1988), small mesh (Gerritsen size is associated with the abilityto ingestsmall (<2 gin) particles(Gophen and Geller 1984, Brendelberger 1985, DeMott 1985). Therefore,small cladocerans probably capture clay particleswith greaterefficiency smallercladocerans thanlargecladocerans. As a result, foralgae, and thusexperience exhibita lowerselectivity a greaterreductionin algal ingestionrate in the presence ofclay. The inability ofsmall cladoceransto avoid ingesting clay particleshas consequences at the population level. Life table experimentshave shown that small,juvenile cladocerans are more susceptiblethan adults to increased mortalityin the presence of susratesofsmaller pended clay,and thepopulationgrowth species are decreased more in the presence of suspended clay than those of largerspecies (Kirk and Gilbert 1990).

terial cells of various nutritional qualities are present 0 along with noxious or toxic cyanobacterialcells and relatively nonnutritious particlessuch as detritus, cal'2) cite crystals, and suspended siltand clay particles(e.g., A 3r 100 Arruda et al. 1983, Melack 1985, Vanderploeg et al. 1987). The abilityof cladocerans to utilize small food ? 80 A particles (<2-5 gin), such as bacteria and nanophyO 60 toplankton, is oftenbeneficial.Nutritiousphytoplankton cells withinthe food-size niche of rotifers (4-18 40 gin) may often be scarce,so thebroaderfood-sizeniche o . of cladocerans (0.5-40 gin) gives them an advantage L20 over rotifers. However, the ability of cladocerans to C 0 . collect small particles,combined with their inability D 20 40 60 80 100 O, 0 to feed selectivelyby sortingnutritiousfromnonnu0 a Decrease in Algal Ingestion Rate (%) tritious particlesafter collection,is disadvantageousin (D thepresenceofsuspendedclay particles.The collection 0 of nonnutritious clay particles causes a reduction in FIG. 5. Relationship inalgalingestion between thechange cells and thus reduces clafeedingon phytoplankton rate (inadult individuals) andthechange inpopulation growth doceran fitness. rate(r,,)inthepresence of50 mg/L suspended clay, for three cladoceran species(A; left to right: Daphniapulex,D. amand Ceriodaphnia bigua, dubia)and three rotifer species(-; Cladoceran bodysize Keratella cochlearis and Synchaeta pectinate on thex axis, Kirk growth ratedatafrom Cladocerans of different body sizes respond differ- and K. crassaabove).Population
and Gilbert(1990). r, = 0.97; P < .01.

and cladocerans to suspended clay. In laboratoryexperimentsusing identicalclay stocksand phytoplankton foods as in the presentstudy,fourcladoceran species (Bosmina longirostris, C. dubia, D. ambigua, and D. pulex) showed 31-100% reductionsin population rate in the presenceof suspended clay. In congrowth trast,the population growthrates of threerotifer species (K. cochlearis,Polyarthra and S. pectinavulgaris, The singlerotifer ta) were unaffected. species thatwas inhibited by suspended clay, K. crassa, experienced only a 30% reductionin population growthrate (Kirk and Gilbert 1990). The reductionsin cladoceran population growthrates are probably caused by the reductionsin thealgal ingestion ratesreported here.When and cladocerans, or when comparcomparingrotifers ing cladoceran species of different body sizes, those species thatshowed greater reductionsin algal feeding rate in the presence of suspended clay also showed greater reductionsin population growth rate (P < .01; Fig. 5). Greater reductionsin algal ingestionrate will resultin less energyand nutrients being available for individual survival and reproduction,and thus will cause greaterreductions in population growth rate. While reductions in the algal ingestion rates of cladocerans can account formuch of the observed reductions in population growthrate, suspended clay also reducestheassimilationefficiency ofingested algal food (Arruda et al. 1983, McCabe and O'Brien 1983). This Mechanistic basis for the change in will also reduce the energyand nutrients available for outcome competitive survival and reproduction. The resultsfrom these short-term experimentson In summary, in the feeding differences modes, foodfeedingbehavior provide a mechanism for the long- size niches,and selectivities ofrotifers and cladocerans termpopulation and communityresponses of rotifers formthe mechanisticbasis forthe change in compet-

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922

KEVIN L. KIRK

Ecology, Vol. 72, No. 3

apparatus itive outcome in the presence of suspended clay. Cla- Geller, W., and H. Muller. 1981. The filtration mesh-sizeand theirimplicationson food and therefore ofCladocera: filter docerans are less selective than rotifers, Oecologia (Berlin) 49:316-321. selectivity. extent.This ingestsuspended clay particlesto a greater J., K. G. Porter,and J. R. Strickler. 1988. Not Gerritsen, of but not reducesalgal ingestionratesof cladocerans, by sieving alone: observations of suspension feeding in The reductionsin algal ingestionrates of clarotifers. Daphnia. Bulletinof Marine Science 43:366-376. Asplanchna: bedocerans reduces their population growthrates, and Gilbert,J. J. 1980. Feeding in the rotifer preydefenses,and impact changes the outcome of competitionbetween rotifers havior,cannibalism,selectivity, on rotifer communities.Pages 158-172 in W. C. Kerfoot, In nature,these and cladocerans in favor of rotifers. editor.Evolutionand ecologyofzooplanktoncommunities. mechanismsmay changethe relativeabundance of roUniversityPress of New England, Hanover, New Hampshire,USA. tifers and cladocerans in zooplankton communities.
ACKNOWLEDGMENTS

I thank Rae Barnhisel, Carol Folt, John Gilbert, Nelson fortheircomments and two anonymousreferees Hairston,Jr., on the manuscript.I am especially indebted to JohnGilbert

Maxine environment. a stimulating laboratory for providing Cory Minor, assistance. Jeff technical excellent Beanprovided analyze theclay.Clyde helped Reynolds and Robert Nislow,
Goulden providedthe Ceriodaphniadubia culture.This study was supportedby the Dartmouth College Cramer Fund, EnvironmentalProtectionAgencygrantR-814210 to J. J. Gilbert and W. C. Kerfoot,and National Science Foundation grantBSR-8415024 to J. J. Gilbert.
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FEEDING AND COMPETITION

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